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* From the Divisions of Infectious Diseases (Drs. Gasink, Blumberg, and Lautenbach, and Ms. Wurcell) and Pulmonary, Allergy and Critical Care, Section of Advanced Lung Disease and Transplantation (Dr. Kotloff), Department of Medicine, University of Pennsylvania, Philadelphia, PA.
Correspondence to: Leanne B. Gasink, MD, Division of Infectious Diseases, 502 Johnson Pavillion, University of Pennsylvania School of Medicine, Philadelphia, PA 19104; e-mail: leanne.gasink{at}uphs.upenn.edu
Abstract
Introduction: Appropriate vaccination status in the pre-solid organ transplant period is critically important.
Methods: To determine if lung transplant candidates are adequately vaccinated for Streptococcus pneumoniae, a cross-sectional study was performed. Electronic records of patients referred to our institution for transplantation evaluation between July 2002 and January 2004 were reviewed.
Results: Only 98 of 157 patients (62.4%; 95% confidence interval [CI], 54.8 to 70.1%) evaluated for lung transplantation reported prior receipt of S pneumoniae vaccine. COPD was the only factor significantly associated with vaccination. Patients with COPD were more likely to have received vaccination compared to patients with other diagnoses (odds ratio, 4.66; 95% CI, 2.26 to 9.60).
Conclusions: S pneumoniae vaccination rates among potential lung transplant candidates fall substantially short of current recommendations for universal immunization. Transplant programs should thoroughly review vaccination status and develop strategies to ensure that candidates receive all appropriate vaccines before transplantation.
Key Words: COPD • solid-organ transplantation • Streptococcus pneumoniae • vaccination
The pretransplant evaluation of a potential solid-organ transplant candidate presents an important opportunity to minimize the risk of posttransplantion infections. In particular, since many vaccinations are more effective when administered prior to the onset of immunosuppression, a full assessment of immunization status and administration of appropriate vaccines, when indicated, is critically important.12 However, since many vaccines are indicated in persons with end-stage organ disease, vaccination status should ideally be up to date at the time of transplant evaluation.
One of several pretransplant immunizations recommended by the American Society of Transplantation is Streptococcus pneumoniae vaccine.1 Vaccination for S pneumoniae is also recommended for patients with chronic lung disease (excluding asthma) and other chronic diseases by the American Committee on Immunization Practices due to an increased risk for severe disease and high mortality.3 The incidence of S pneumoniae infection is higher in organ transplant populations compared to normal hosts, presumably due to their immunosuppressed state. Data support much higher rates in heart transplant recipients (36/1,000 patient-years) and renal transplant recipients (28 infections/1,000 patient-years) than in the general population (0.24/1,000 patient-years).456 In lung transplant candidates and recipients who already have diminished respiratory reserve, infection may result in more severe disease with a higher frequency of respiratory failure and death, even when compared to other comparable immunosuppressed patients.
Despite the potential implications of not receiving S pneumoniae vaccination in the pretransplant period, the extent to which health-care providers adequately vaccinate patients who may ultimately receive an organ transplant is completely unknown. An assessment of compliance with current recommendations is necessary so that transplant centers can take the necessary steps to ensure universal vaccination of all lung transplant candidates.
Materials and Methods
A cross-sectional study was performed at the Lung Transplant Center at the Hospital of the University of Pennsylvania and included all potential lung transplant candidates evaluated for transplantation between July 1, 2002, and January 31, 2004. The study was approved by the Committee on Studies Involving Human Beings of the University of Pennsylvania.
Candidates deemed suitable for further evaluation after review of medical records from the referring physician and an initial visit in the Lung Transplant Clinic are scheduled for a 3-day, formal evaluation process. Results of this evaluation and the initial visit are consolidated into a Lung Transplant Evaluation Summary, which is available electronically and in hard copy in each patient’s individual chart. In general, patients referred for formal evaluation are < 64 years old with advanced, nonmalignant diseases of the lungs who are at high risk of death in the subsequent several years. Information included in the evaluation summary includes basic demographic information, history of present illness, medical history, medications, social history, family history, physical examination, and results of pulmonary, cardiac, gynecologic, dental, laboratory, and immunologic evaluations, as well as consultations and special tests as deemed necessary. A subsection devoted to immunization history is included in the medical history portion of the evaluation summary form. Information regarding types and timing of vaccination against influenza, S pneumoniae, and other immunizations are recorded according to patient self-report and/or available medical records. Evaluation summaries were reviewed in order to ascertain the S pneumoniae vaccination status for all patients undergoing evaluation during the study period and to identify predictors of vaccination.
We identified all patients evaluated during the study period and determined the proportion of persons who had received vaccination. Data collected included age, sex, race, etiology of lung disease, presence of diabetes mellitus and/or cardiac disease, and date of referral for transplant evaluation. Bivariable analyses were performed to identify the association between potential risk factors and prior receipt of S pneumoniae vaccination. 
2 analysis was used for categorical variables, while the Student t test or Wilcoxon rank-sum test were used for continuous variables.7 Variables with a p value 
0.2 were included in a multivariable analysis. A two-tailed p value < 0.05 was considered significant. All statistical analysis was performed using statistical software (STATA 8.0 software; Stata Corporation; College Station, TX).
Results
During the study period, 157 patients underwent formal evaluation for lung transplantation. The median age at time of referral to the lung transplant clinic was 54 years (interquartile range, 47 to 59 years). The majority of patients were men (n = 81 [51.6%]) and white (n = 127 [80.9%]). Twenty-two patients (14.0%) were African American. Diagnoses included COPD in 72 patients (45.9%), idiopathic pulmonary fibrosis (IPF) in 41 patients (26.1%), cystic fibrosis in 11 patients (7.0%), primary pulmonary hypertension in 9 patients (5.7%), 
1-antitrypsin deficiency in 5 patients, and other diagnoses in 12 patients. Thirteen patients reported a history of cardiac disease, and 9 patients had diabetes mellitus.
Receipt of S pneumoniae vaccination was reported in 98 evaluated patients (62.4%; 95% confidence interval [CI], 54.8 to 70.1%). Vaccination was reported in 80.6% of persons with COPD, 43.9% of persons with IPF, and 36.4% of persons with cystic fibrosis. As shown in Table 1 , persons with COPD were significantly more likely to have received vaccination. Age, sex, race, presence of cardiac disease or diabetes mellitus, and time of referral were not significantly associated with vaccination status. In multivariable analyses, COPD remained the only significant factor associated with vaccination status (adjusted odds ratio, 4.75; 95% CI, 2.17–10.41).
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Although the importance of vaccination has been emphasized by the American Committee on Immunization Practices and the American Society of Transplantation, only 62% of patients with chronic pulmonary disease who were evaluated for lung transplantation at our institution had received appropriate immunization for S pneumoniae.13 Patients with diagnoses other than COPD were less likely to have received vaccination, calling into question physicians’ appreciation of the importance of vaccination in all potential lung transplant candidates, regardless of etiology.
Our findings are consistent with published data in other populations. Despite goals set by the Centers for Disease Control and Prevention, whose target vaccination rate is 90% by 2010, only 56% of persons > 65 years old were vaccinated for S pneumoniae in 2002.8 Furthermore, it is estimated that only 20% of persons aged 50 to 64 years with chronic illnesses meeting vaccination criteria receive immunization.3
The observed prevalence of vaccination in our study falls substantially short of universal vaccination and is quite surprising given the population studied. Patients considered for transplantation are generally motivated patients for whom every effort is being made to provide a prolonged high quality of life. They are subjected to rigorous screening and vigilant care to ensure optimal pretransplant health and prevent deterioration prior to transplantation. Large amounts of resources are devoted to transplant candidates in order to maximize utilization of scarce organs and transplant outcomes, including infectious complications. This may be particularly true for lung transplant candidates given the strict eligibility criteria, paucity of available organs, and inferior outcomes compared to other solid-organ transplants.
Although the reasons for inadequate vaccination in our study cohort are unknown, frequent sick visits that shift attention away from health maintenance; fragmented care between primary physicians and multiple specialists; concerns about side effects from vaccines; the sometimes overwhelming psychological stress associated with a chronic, life-threatening illness; and the potential for an underappreciation by physicians and patients of the importance of S pneumoniae vaccination are possible barriers to immunization. The increased likelihood of vaccination among patients with COPD may reflect a greater number of opportunities to vaccinate given the frequently prolonged course of illness compared to other diagnoses such as IPF. However, it may also reflect a greater perceived risk of S pneumoniae infection among these individuals and an inadequate recognition of the importance of vaccination in all patients with advanced lung disease.
This study has several limitations. Our findings represent only a single-center experience, although subjects were referred from a variety of physicians within a wide geographic area. We did not determine if unvaccinated patients ultimately received vaccination prior to transplantation, but this will undoubtedly vary from center to center. Finally, the validity of patient self-report has not been established in lung transplant patients. Data from other populations, however, suggest that patient self-report actually underestimates the true prevalence. Two studies910 have investigated the validity of patient self-report of pneumococcal vaccination in elderly populations and found the sensitivity and specificity of patient self-reported S pneumoniae vaccination to be 85 to 100% and 46 to 79%, respectively. Thus, the ability to correctly recall having received S pneumoniae vaccination may be much better than correctly recalling not having received vaccination, suggesting that the problem of undervaccination may be even more prevalent than our results suggest.
In summary, fewer than two thirds of patients with chronic lung diseases referred to our institution for lung transplantation evaluation reported receipt of S pneumoniae vaccination. Vaccination in lung transplant candidates is critically important because patients may have a higher risk of severe infection and a decreased response to vaccination after transplantation. We urge lung transplant programs to make every attempt to ensure universal vaccination and confirm self-report of vaccination through medical records. There is a need to identify obstacles to immunization, educate physicians and patients on the importance of vaccination, and develop strategies to optimize vaccination rates for all transplant candidates.
Footnotes
Abbreviations: CI = confidence interval; IPF = idiopathic pulmonary fibrosis
Presented in part at the American Transplant Congress, Seattle WA, May 20–23, 2005 (abstract 250599).
This work was supported by Public Health Service grant DK-02987-01 of the National Institutes of Health (Dr. Lautenbach).
Received for publication November 18, 2005. Accepted for publication January 7, 2006.
References
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